VThunter: a database for single-cell screening of virus target cells in the animal kingdom
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Nucleic Acids Research, 2021 1
https://doi.org/10.1093/nar/gkab894
VThunter: a database for single-cell screening of virus
target cells in the animal kingdom
Dongsheng Chen 1,2,*,† , Cong Tan1,† , Peiwen Ding1,2,† , Lihua Luo1,2,† , Jiacheng Zhu1,2,† ,
Xiaosen Jiang1,2,† , Zhihua Ou1,3 , Xiangning Ding1,2 , Tianming Lan1,2 , Yixin Zhu1,2 , Yi Jia1 ,
Yanan Wei1,4 , Runchu Li1,4 , Qiuyu Qin1,4 , Chengcheng Sun 1,2 , Wandong Zhao1,4 ,
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Zhiyuan Lv1,4 , Haoyu Wang1,2 , Wendi Wu1,4 , Yuting Yuan1,5 , Mingyi Pu1,4 , Yuejiao Li1 ,
Yanan Zhang1,6 , Ashley Chang1 , Guoji Guo7 , Yong Bai1,* , Xin Jin1,8,9,* and Huan Liu1,2,*
1
BGI-Shenzhen, Shenzhen 518083, China, 2 College of Life Sciences, University of Chinese Academy of Sciences,
Beijing 100049, China, 3 Shenzhen Key Laboratory of Unknown Pathogen Identification, BGI-Shenzhen, Shenzhen
518083, China, 4 School of Basic Medicine, Qingdao University, Qingdao 266071, China, 5 Department of Physiology,
School of Basic Medical Sciences, Binzhou Medical University, Yantai 264003, China, 6 Tsinghua-Berkeley Shenzhen
Institute (TBSI), Tsinghua University, Shenzhen, 518055, China, 7 Center for Stem Cell and Regenerative Medicine,
Zhejiang University School of Medicine, Hangzhou 310058, China, 8 School of Medicine, South China University of
Technology, Guangzhou 510006, Guangdong, China and 9 Guangdong Provincial Key Laboratory of Human Disease
Genomics, Shenzhen Key Laboratory of Genomics, BGI-Shenzhen, Shenzhen 518083, China
Received August 14, 2021; Revised September 11, 2021; Editorial Decision September 18, 2021; Accepted October 05, 2021
ABSTRACT natures of viral receptors. VThunter offers an infor-
mative and convenient resource for scientists to bet-
Viral infectious diseases are a devastating and con-
ter understand the interactions between viral recep-
tinuing threat to human and animal health. Recep-
tors and animal viruses and to assess viral patho-
tor binding is the key step for viral entry into host
genesis and transmission in species. Database URL:
cells. Therefore, recognizing viral receptors is funda-
https://db.cngb.org/VThunter/.
mental for understanding the potential tissue tropism
or host range of these pathogens. The rapid ad-
vancement of single-cell RNA sequencing (scRNA- INTRODUCTION
seq) technology has paved the way for studying
The COVID-19 pandemic has caused huge loss of human
the expression of viral receptors in different tissues
life, economic recession, and social disruption worldwide,
of animal species at single-cell resolution, result- underscoring the destructive impact of infectious diseases
ing in huge scRNA-seq datasets. However, effec- on human health and global security. Severe acute respi-
tively integrating or sharing these datasets among ratory syndrome coronavirus 2 (SARS-CoV-2) can infect
the research community is challenging, especially various animals, including bats, pangolins, cats, dogs, fer-
for laboratory scientists. In this study, we manu- rets and minks (1–6). With the occurrence of anthropogenic
ally curated up-to-date datasets generated in ani- transmission of SARS-CoV-2 to animals, the potential host
mal scRNA-seq studies, analyzed them using a uni- range of this virus continues to raise concerns within the
fied processing pipeline, and comprehensively an- scientific community. Moreover, the emergence of SARS-
notated 107 viral receptors in 142 viruses and ob- CoV-2 also highlights the need for more rapid host range
tained accurate expression signatures in 2 100 962 identification upon the emergence of novel pathogens.fun
In recent decades, tremendous achievements have been
cells from 47 animal species. Thus, the VThunter
made to characterize the host range and tissue tropism of
database provides a user-friendly interface for the viruses using traditional methods like epidemiological in-
research community to explore the expression sig- vestigations or animal infection experiments. While these
* To
whom correspondence should be addressed. Tel: +86 755 33945563; Fax: +86 755 32960023; Email: liuhuan@genomics.cn
Correspondence may also be addressed to Dongsheng Chen. Email: dschen2016@gmail.com
Correspondence may also be addressed to Xin Jin. Email: jinxin@genomics.cn
Correspondence may also be addressed to Yong Bai. Email: baiyong@genomics.cn
†
The authors wish it to be known that, in their opinion, the first six authors should be regarded as Joint First Authors.
C The Author(s) 2021. Published by Oxford University Press on behalf of Nucleic Acids Research.
This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial License
(http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work
is properly cited. For commercial re-use, please contact journals.permissions@oup.com
2 Nucleic Acids Research, 2021
approaches are essential to elucidate bona fide viral infec- VThunter is a-value-added database with transformative in-
tion in animals, it is impossible to carry out large-scale formation to facilitate study of the cross-species transmis-
screening on the versatile species that might be suscep- sion mechanisms of animal viruses.
tible to this pathogen, due to the limited availability of
virus/animal/experimental resources. Recent advances in
DATA COLLECTION AND DATABASE CONTENT
scRNA-seq technology has opened up new ways to identify
all cell types in various tissues and/or organs and profile In total, 285 animal scRNA-seq datasets generated from
gene expression landscapes at single cell resolution, which 2 100 962 cells in 47 animal species were collected and
holds tremendous potential to predict the potential cell used to predict the cell types targeted by viruses (Figure
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types, tissues and organs targeted by viruses based on the 1A, Supplementary Data 1 and Supplementary Data 2).
expression profiles of their receptors in all cell types. For The list of these 285 scRNA-Seq datasets is available on
example, we conducted scRNA-seq for 11 representative the database ‘Download’ page, and includes detailed meta-
species in pets, livestock, poultry, and wildlife to build the data for each dataset, such as data source, time, technol-
expression pattern profiles of all cell types to screen the po- ogy, species name, sample tissue, treatment, cell number and
tential target cell types and hosts of SARS-CoV-2 in a previ- URL for related literature. scRNA-seq datasets were re-
ous study (7), where cats were found to be highly susceptible trieved based on literature search and downloaded from
to SARS-CoV-2, in accordance with serological and exper- multiple scRNAseq data repositories including Gene Ex-
imental findings by other researchers (3,6,8). Because cellu- pression Omnibus (NCBI/GEO) (11), Human Cell Atlas
lar receptors play a critical role in the cell entry process of Portal (HCA) (16), Single Cell Expression Atlas (EMBL-
virus, identifying the tissue tropism is the first step towards EBI/SCEA) (17) and Mouse Cell Atlas (MCA) (18). The
understanding the pathogenesis and transmission of viruses information of receptor information of 142 animal viruses
in different hosts, thus laying the foundation for the preven- were obtained from the Viral Receptor database (19) and
tion and control of putative outbreaks (9). Predicting host UniProt (20) (Supplementary Data 3).
and tissue tropism based on comprehensive gene expression All the literatures of the studies generating the above
patterns at single-cell resolution is promising but presents scRNA-seq datasets were manually confirmed by a group
challenges for laboratory biologists and experimentalists as of experienced researchers and all the scRNA-seq dataset
the huge amount of data obtained from scRNA-seq stud- were processed with a unified analyzing pipeline (Figure
ies can be daunting for those with limited backgrounds in 1B). Briefly, they are processed with steps composed of both
bioinformatics. utilities packaged in Seurat v3.0 and in-house scripts ac-
Several databases have been developed to make avail- cording to previously study (21,22). Firstly, we conduct the
able the rapidly increasing volume of scRNA-seq data. Raw quality control by filtering out cells with expressed genes
data and expression matrix datasets produced in scRNA-
Nucleic Acids Research, 2021 3
A
Single-cell Data Collection
Snake Lung
Human Chicken Respiratory system
Reptiles Colon
Lizard Digestive system
Mouse Duck Liver
Turtle Cardiovascular system Pancreas
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Monkey Goose
Urinary system PBMC
Pig Pigeon Zebrafish Fishes Heart
Integumentary system
Species Bat Pelican Systems Kidney Tissues
Skeletal system
Skin
Hamster Black Necked Crane
(47) Muscular system Adipose
Rabbit Blue Peacock
Drosophila Insects
Endocrine system Bone
Mongolian Horse Sun Conure Lymphatic system Testes
Caenorhabditis elegans
Deer Guinea Fowl Nervous system Spleen
Sea urchin Others Brain
...... ...... ...... Reproductive system
Retina
...... ......
Mammals Birds
Virus Collection
23 Families .......
107 Receptors
B
Data Processing
Homologous genes Metadata
Quality control Normalization Clustering
converting reconstruction
(Species to Human) (min.cells = 1, min.features = 200) (Species, Tissues, Cell Types)
C
User interface
VThunter
Virus Spectrum Host Spectrum Co-expression Download
Virus Hosts Species Raw Data
Receptor Genes Tissues Gene1 Gene2 Gene3 …… Processed Data
Hosts Tropism Cell Types Co-expression Query Meta Data
Tissues Tropism Receptor Genes Expression Barplot of co-expression
Cell Types Tropism Virus Featureplot of receptors
Figure 1. Overview of data collection, data processing and functional modules of VThunter database. (A) Diagram of species and tissues of collected
scRNA-Seq datasets. (B) Steps of unified pipeline to process the curated scRNA-Seq datasets. (C) Overview of functional modules and user interfaces.
4 Nucleic Acids Research, 2021
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Figure 2. Statistics of viruses of receptors and animal species with scRNA-Seq datasets in this database. Pie chart showing the percentage of viruses of
curated receptors according to their strand type (A), viruses of curated receptors according to their family type (B), according to their receptors (C),
curated scRNA-Seq datasets according to species classification (D), curated scRNA-Seq datasets according to species system (E), curated scRNA-Seq
datasets according to organs (F).
users to the functional interfaces. On the ‘Home’ page, there APPLICATION CASE
are four main elements in addition to the header and navi-
VThunter is a comprehensive database designed for virolog-
gation menu, including search forms for virus receptors or
ical study, where users can search for viruses of interest to
virus target genes, galleries for representative viral and an-
obtain information on host tropism, including target tissues
imal species, and statistics related to data resources main-
and cell types in certain animal species, and to investigate
tained by VThunter (Figure 2). If users are interested with
viruses potentially infecting an animal species.
searching the host spectrum of certain virus, they could
If a researcher wonders what animal species may be tar-
query the virus in the search box or select it in the virus
geted by Rabies lyssavirus, they could conduct the following
gallery to enter a virus page with comprehensive informa-
steps to obtain the relevant information as shown in Figure
tion of viral receptor and host tropism including target
3: (i) Select ‘Rhabdoviridae’ in virus family option list → se-
genes and target species with the expression profiles of the
lect ‘Rabies lyssavirus’ in virus option list → select ‘GRM2’
target genes in tissues and cell types. If a researcher only
→ click ‘Search’. (ii) (optional) Find the Rabies lyssavirus
wants to fucus on a specific animal species, they could select
in the representative virus gallery or in the ‘Virus Spectrum’
the species of interest in the animal species gallery and enter
page, then click the ‘Check Details’ button under the virus
an animal species page where receptor expression profiles
icon. (iii) Users will be guided to the virus tropism page. In
of all viruses that may potentially infect that animal species
this page, animals with expression record of GRM2 will be
will be present.
displayed. If we click on the ‘Check Details’ button on the
On the ‘Virus Spectrum’ page, users could browse all the
right of a specific animal, such as civet, the taxonomy lin-
viruses with comprehensive receptor and host tropism in-
eage information for civet and the literature-based general
formation collected in this database. The ‘Check Details’
information about Rabies lyssavirus and its infecting recep-
button under a virus icon will lead users to the virus page
tor are provided. All the scRNA-seq datasets collected in
(Figure 3). Similarly, users could select a certain animal
this database and relevant metadata including tissue type,
species in the ‘Host Spectrum’page and click the ‘Check
animal health status, experimental details will be given in
Details’ button under the species icon to enter an animal
a data source form. After choosing a certain dataset, tak-
species page (Figure 4). On the ‘Demo’ page, users can
ing ‘Vthunter 007’ for example, an overall cell type cluster
quickly view the content and format of data retrievable
figure will be displayed on the left and the gene expression
from VThunter. In the ‘Download’ page, links of all the
of gene GRM2 in each cell types will be displayed on the
raw data and resultant files maintained in this database are
right. Furthermore, a boxplot showing the expression level
provided for interested researchers to conduct further anal-
of gene GRM2 in different tissues of civet will also be pro-
ysis to meet their personalized needs. In the ‘Help’ page,
vided.
a graphical operation guide is prepared for new users to
In addition to querying host tropism for a certain virus,
get used to query relevant information easily, which will
we may also want to know which viruses can affect the
help them fully use the resource in VThunter. Besides, the
health of a certain animal species. Here, we take cat as the
‘Co-expression’ module is also implemented for further in-
animal of interest (Figure 4). Briefly, our search process in-
spect the co-expression genes of the certain viral receptors
volves three steps: (i) click on the cat specie icon in the rep-
based on the comprehensive scRNA-seq expression profiles
resentative galley in the homepage, or, enter the ‘Host Spec-
in VThunter (Figure 5).
trum’ page → select ‘Mammals’ in the classification option
Nucleic Acids Research, 2021 5
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Figure 3. Demonstration of Virus Spectrum module. (A) Searching for virus via ‘Home’ page or ‘Virus spectrum’. (B) Operation to obtain detail information
in virus page. (C) Screenshot of virus information page. (D) Operation to view different receptor information of each virus in virus page. (E, F) Operation
and screenshot of checking scRNA-seq expression profile of viral receptors.
6 Nucleic Acids Research, 2021
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Figure 4. Demonstration of Host Spectrum module. (A) Screenshot of searching animal species via ‘Home’ page or ‘Host spectrum’ page. (B) Operation to
check detail information of certain species. (C) Screenshot of species information page. (D) Operation to check information of potential viruses in species
page. (E, F) Operation and screenshot of checking scRNA-seq expression profile of virus receptors in species page.
Nucleic Acids Research, 2021 7
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Figure 5. Demonstration of gene co-expression module. (A–D) Operations to enter ‘Co-expression’ page and perform co-expression query. (E) Screenshot
of co-expression information of given genes.
8 Nucleic Acids Research, 2021
list and select ‘Cat’ in the species option list → click ‘Search’ ACKNOWLEDGEMENTS
→ enter the cat page (ii) in this page, you could have an
The authors would like to thank Dr Lei Chen and Dr Yi-
overview of what viruses might attack cat, what genes be
quan Wu for constructive suggestion and feedback from
targeted as the receptor and what tissues of cat have the ex-
users.
pression of the target genes. (iii) After clicking the link of
target gene ‘ACE2’ as the receptor of SARS-CoV-2, users
will be led to the page showing the details of scRNA-seq FUNDING
studies conducted on cat and the expression levels of ACE2
in each cell type and different tissues. Funding for open access charge: Self-funding.
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The above simple search steps highlight the user-friendly Conflict of interest statement. None declared.
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